NEW MICROBES IN HUMANS
Cutaneous infection and bactaeremia caused by Erwinia billingiae: a case report M. Prod’homme1, L. A. Micol1, S. Weitsch1, J.-L. Gassend1, O. Martinet1 and C. Bellini2
Erwinia billingiae is a Gram-negative bacteria belonging to the Enterobacteriaceae family which is usually pathogenic to plants [8]. Human infections by Erwinia-like microorganisms are rarely described. The first case reported in the literature was that of an 88-year-old woman with a urinary tract infection related to Erwinia persicinus [9]. The second case concerned a 79-year-old woman with cervical lymphadenitis caused by an Erwinia tasmaniensis–like organism [10].
1) General Surgery Department and 2) Infectious Diseases Department, Riviera-Chablais Hospital, Montreux, Switzerland
Abstract Cellulitis and erysipelas are common skin infections usually caused by Staphylococcus aureus and streptococci. Gram-negative rods are rarely implicated. We report here a case of dermohypodermitis and bactaeremia caused by Erwinia billingiae, a Gram-negative bacteria usually pathogenic and epiphytic to pome fruit tree. © 2017 The Authors. Published by Elsevier Ltd. Keywords: Bloodstream infection, dermohypodermitis, Erwinia billingiae, erysipelas, lymphangitis Original Submission: 18 June 2017; Revised Submission: 11 July 2017; Accepted: 13 July 2017 Article published online: 23 July 2017
Corresponding author: M. Prod’homme, Hôpital Riviera-Chablais, Avenue de Belmont 5, 1820 Montreux, Switzerland E-mail: [email protected]
Introduction Acute bacterial skin infections like cellulitis and erysipelas are common skin infections, with an incidence rate of 1/1000 per year [1]. They are usually caused by aerobic Gram-positive bacteria, such as Staphylococcus aureus and group A β-haemolytic streptococci, and only rarely by Gram-negative bacteria such as Pseudomonas aeruginosa and other enterobacteria (i.e. Klebsiella spp., Proteus mirabilis) [2–5]. Common risk factors include lymphoedema, disruption of the cutaneous barrier and toe–web intertrigo [6]. Blood cultures are positive in about 5 to 10% of cases [5,7].
Case presentation In July 2015, a 40-year-old man with known chronic hepatitis C sought care at our emergency department with a painful redness of his third right toe which was rapidly spreading to the back of his foot. It had appeared the previous day after a barefoot walk in the grass. He did not complain of shivering or fever. There was no history of clear trauma or insect bite. Examination revealed a painful, diffuse oedema and redness of his third toe and the back of his foot (Fig. 1A), compatible with dermohypodermitis and associated with lymphangitic streaking up to the medial calf (Fig. 1B), as well as painful and swollen popliteal and inguinal lymph nodes. The interdigital space showed lesions suggestive of intertrigo. He did not manifest other local or general symptoms. Conventional X-rays of the foot did not reveal an underlying bone injury or the presence of foreign bodies. Blood culture samples and skin squames were collected. According to local guidelines, an empiric antibiotic treatment with amoxicillin–clavulanic acid (first dose 2.2 g iv followed by 1 g twice a day orally) was started [1,10]. In addition, the patient’s right leg and foot were immobilized in a posterior cast. We prescribed once-daily thromboprophylaxis with subcutaneous dalteparin sodium 5000 IU and a systemic nonsteroidal anti-inflammatory drug (ibuprofen) with no weight bearing permitted. One out of two pairs of blood cultures grew Erwinia billingiae. Antibiogram revealed resistance to all β-lactam antibiotics except carbapenems, intermediary resistance to gentamicin, and sensitivity to ciprofloxacin and cotrimoxazole. Furthermore, the local samples of his intertoe compartments revealed the presence of the dermatophyte Trichophyton rubrum. Because of the results of the susceptibility testing, antibiotic treatment was changed to oral ciprofloxacin 500 mg twice daily and continued for 14 days. Further clinical evolution was favourable: the patient did not report any additional fever, and the local redness, oedema and pain rapidly resolved. At follow-up 2 months later, the patient remained asymptomatic and without any sequelae.
New Microbe and New Infect 2017; 19: 134–136 © 2017 The Authors. Published by Elsevier Ltd This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) http://dx.doi.org/10.1016/j.nmni.2017.07.006
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FIG. 1. Initial clinical presentation. (A) Redness of third toe and over back of foot. (B) Lymphangitic redness up to medial calf (marked in blue).
directed antibiotic therapy suggests a possible implication of this Erwinia strain as an opportunistic agent in this infection.
Discussion To our knowledge, this is the first case of human infection caused by Erwinia billingiae reported in the literature. Erwinia billingiae is a Gram-negative bacterial strain belonging to the Enterobacteriaceae family, first described in 1999 [11]. Species in this genus are similar to Pantoea and Enterobacter species, and many Erwinia species have been reclassified into these groups [8,12]. Usually Erwinia species are plant-associated bacteria, pathogenic or not [13–15]. Pathogenic species like Erwinia amylovora and Erwinia pyrifoliae are connected with so-called pome fruit diseases (i.e. the fire blight of apples), while species like E. tasmaniensis and E. billingiae are rather epiphytic, nonpathogenic bacteria [16]. Clinical isolates of Erwinia spp. are rare: Erwinia persicina was isolated from the urine of a woman with a urinary tract infection [9], and E. tasmaniensis was found in a biopsy tissue sample of cervical lymphadenitis [10]. Other case reports describe Erwinia spp. as a possible causative agent of urinary tract infections [17]. However, it is not clear if the organism actually caused the infection. In the present case the patient exhibited dermohypodermitis associated with bloodstream infection due to Erwinia billingiae. Our hypothesis is that the interdigital intertrigo and the barefoot walk in a grassy field were the risk factors for this infection. Even if a skin biopsy demonstrating bacterial growth was not performed, the favourable clinical course after receipt of
Conflict of interest None declared.
References [1] Gabillot-Carre M, Roujeau JC. Acute bacterial skin infections and cellulitis. Curr Opin Infect Dis 2007;20:118–23. [2] Semel JD, Goldin H. Association of athlete’s foot with cellulitis of the lower extremities: diagnostic value of bacterial cultures of ipsilateral interdigital space samples. Clin Infect Dis 1996;23:1162–4. [3] Peralta G, Padrón E, Roiz MP, De Benito I, Garrido JC, Talledo F, et al. Risk factors for bacteremia in patients with limb cellulitis. Eur J Clin Microbiol Infect Dis 2006;25:619–26. [4] Carratala J, Roson B, Fernandez-Sabe N, Shaw E, Del Rio O, Rivera A, et al. Factors associated with complications and mortality in adult patients hospitalized for infectious cellulitis. Eur J Clin Microbiol Infect Dis 2003;22:151–7. [5] Gunderson CG, Martinello RA. A systematic review of bacteremias in cellulitis and erysipelas. J Infect 2012;64:148–55. [6] Dupuy A, Benchikhi H, Roujeau JC, Bernard P, Vaillant L, Chosidow O, et al. Risk factors for erysipelas of the leg (cellulitis): case–control study. BMJ 1999;318(7198):1591–4. [7] Perl B, Gottehrer NP, Raveh D, Schlesinger Y, Rudensky B, Yinnon AM. Cost-effectiveness of blood cultures for adult patients with cellulitis. Clin Infect Dis 1999;29:1483–8.
© 2017 The Authors. Published by Elsevier Ltd, NMNI, 19, 134–136 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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[8] Llop P. Genetic islands in pome fruit pathogenic and non-pathogenic Erwinia species and related plasmids. Front Microbiol 2015:6. [9] O’Hara CM, Steigerwalt AG, Hill BC, Miller JM, Brenner DJ. First report of a human isolate of Erwinia persicinus. J Clin Microbiol 1998;36: 248–50. [10] Shin SY, Lee MY, Song JH, Ko KS. New Erwinia-like organism causing cervical lymphadenitis. J Clin Microbiol 2008;46:3156–8. [11] Bläckberg A, Trell K, Rasmussen M. Erysipelas, a large retrospective study of aetiology and clinical presentation. BMC Infect Dis 2015;15:1. [12] Hauben L, Moore ER, Vauterin L, Steenackers M, Mergaert J, Verdonck L, et al. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 1998;21:384–97. [13] Stevens DL, Bisno AL, Chambers HF, Everett ED, Dellinger P, Goldstein EJ, et al. Practice guidelines for the diagnosis and
[14]
[15]
[16]
[17]
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management of skin and soft-tissue infections. Clin Infect Dis 2005;41: 1373–406. Mergaert J, Hauben L, Cnockaert MC, Swings J. Reclassification of nonpigmented Erwinia herbicola strains from trees as Erwinia billingiae sp. nov. Int J Syst Bacteriol 1999;49:377–83. Palacio-Bielsa A, Roselló M, Llop P, López MM. Erwinia spp. from pome fruit trees: similarities and differences among pathogenic and nonpathogenic species. Trees 2012;26:13–29. Kube M, Migdoll AM, Gehring I, Heitmann K, Mayer Y, Kuhl H, et al. Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genomics 2010;11:393. Umenai T, Saitoh Y, Takano S, Shoji E, Tanaka K, Ishida N. Significance of Erwinia in the vagina as causative agents of urinary tract infections. Tohoku J Exp Med 1979;129:103–4.
© 2017 The Authors. Published by Elsevier Ltd, NMNI, 19, 134–136 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Cutaneous infection and bactaeremia caused by Erwinia billingiae: a case report M. Prod’homme1, L. A. Micol1, S. Weitsch1, J.-L. Gassend1, O. Martinet1 and C. Bellini2
Erwinia billingiae is a Gram-negative bacteria belonging to the Enterobacteriaceae family which is usually pathogenic to plants [8]. Human infections by Erwinia-like microorganisms are rarely described. The first case reported in the literature was that of an 88-year-old woman with a urinary tract infection related to Erwinia persicinus [9]. The second case concerned a 79-year-old woman with cervical lymphadenitis caused by an Erwinia tasmaniensis–like organism [10].
1) General Surgery Department and 2) Infectious Diseases Department, Riviera-Chablais Hospital, Montreux, Switzerland
Abstract Cellulitis and erysipelas are common skin infections usually caused by Staphylococcus aureus and streptococci. Gram-negative rods are rarely implicated. We report here a case of dermohypodermitis and bactaeremia caused by Erwinia billingiae, a Gram-negative bacteria usually pathogenic and epiphytic to pome fruit tree. © 2017 The Authors. Published by Elsevier Ltd. Keywords: Bloodstream infection, dermohypodermitis, Erwinia billingiae, erysipelas, lymphangitis Original Submission: 18 June 2017; Revised Submission: 11 July 2017; Accepted: 13 July 2017 Article published online: 23 July 2017
Corresponding author: M. Prod’homme, Hôpital Riviera-Chablais, Avenue de Belmont 5, 1820 Montreux, Switzerland E-mail: [email protected]
Introduction Acute bacterial skin infections like cellulitis and erysipelas are common skin infections, with an incidence rate of 1/1000 per year [1]. They are usually caused by aerobic Gram-positive bacteria, such as Staphylococcus aureus and group A β-haemolytic streptococci, and only rarely by Gram-negative bacteria such as Pseudomonas aeruginosa and other enterobacteria (i.e. Klebsiella spp., Proteus mirabilis) [2–5]. Common risk factors include lymphoedema, disruption of the cutaneous barrier and toe–web intertrigo [6]. Blood cultures are positive in about 5 to 10% of cases [5,7].
Case presentation In July 2015, a 40-year-old man with known chronic hepatitis C sought care at our emergency department with a painful redness of his third right toe which was rapidly spreading to the back of his foot. It had appeared the previous day after a barefoot walk in the grass. He did not complain of shivering or fever. There was no history of clear trauma or insect bite. Examination revealed a painful, diffuse oedema and redness of his third toe and the back of his foot (Fig. 1A), compatible with dermohypodermitis and associated with lymphangitic streaking up to the medial calf (Fig. 1B), as well as painful and swollen popliteal and inguinal lymph nodes. The interdigital space showed lesions suggestive of intertrigo. He did not manifest other local or general symptoms. Conventional X-rays of the foot did not reveal an underlying bone injury or the presence of foreign bodies. Blood culture samples and skin squames were collected. According to local guidelines, an empiric antibiotic treatment with amoxicillin–clavulanic acid (first dose 2.2 g iv followed by 1 g twice a day orally) was started [1,10]. In addition, the patient’s right leg and foot were immobilized in a posterior cast. We prescribed once-daily thromboprophylaxis with subcutaneous dalteparin sodium 5000 IU and a systemic nonsteroidal anti-inflammatory drug (ibuprofen) with no weight bearing permitted. One out of two pairs of blood cultures grew Erwinia billingiae. Antibiogram revealed resistance to all β-lactam antibiotics except carbapenems, intermediary resistance to gentamicin, and sensitivity to ciprofloxacin and cotrimoxazole. Furthermore, the local samples of his intertoe compartments revealed the presence of the dermatophyte Trichophyton rubrum. Because of the results of the susceptibility testing, antibiotic treatment was changed to oral ciprofloxacin 500 mg twice daily and continued for 14 days. Further clinical evolution was favourable: the patient did not report any additional fever, and the local redness, oedema and pain rapidly resolved. At follow-up 2 months later, the patient remained asymptomatic and without any sequelae.
New Microbe and New Infect 2017; 19: 134–136 © 2017 The Authors. Published by Elsevier Ltd This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) http://dx.doi.org/10.1016/j.nmni.2017.07.006
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Prod’homme et al.
Erysipelas caused by Erwinia billingiae
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FIG. 1. Initial clinical presentation. (A) Redness of third toe and over back of foot. (B) Lymphangitic redness up to medial calf (marked in blue).
directed antibiotic therapy suggests a possible implication of this Erwinia strain as an opportunistic agent in this infection.
Discussion To our knowledge, this is the first case of human infection caused by Erwinia billingiae reported in the literature. Erwinia billingiae is a Gram-negative bacterial strain belonging to the Enterobacteriaceae family, first described in 1999 [11]. Species in this genus are similar to Pantoea and Enterobacter species, and many Erwinia species have been reclassified into these groups [8,12]. Usually Erwinia species are plant-associated bacteria, pathogenic or not [13–15]. Pathogenic species like Erwinia amylovora and Erwinia pyrifoliae are connected with so-called pome fruit diseases (i.e. the fire blight of apples), while species like E. tasmaniensis and E. billingiae are rather epiphytic, nonpathogenic bacteria [16]. Clinical isolates of Erwinia spp. are rare: Erwinia persicina was isolated from the urine of a woman with a urinary tract infection [9], and E. tasmaniensis was found in a biopsy tissue sample of cervical lymphadenitis [10]. Other case reports describe Erwinia spp. as a possible causative agent of urinary tract infections [17]. However, it is not clear if the organism actually caused the infection. In the present case the patient exhibited dermohypodermitis associated with bloodstream infection due to Erwinia billingiae. Our hypothesis is that the interdigital intertrigo and the barefoot walk in a grassy field were the risk factors for this infection. Even if a skin biopsy demonstrating bacterial growth was not performed, the favourable clinical course after receipt of
Conflict of interest None declared.
References [1] Gabillot-Carre M, Roujeau JC. Acute bacterial skin infections and cellulitis. Curr Opin Infect Dis 2007;20:118–23. [2] Semel JD, Goldin H. Association of athlete’s foot with cellulitis of the lower extremities: diagnostic value of bacterial cultures of ipsilateral interdigital space samples. Clin Infect Dis 1996;23:1162–4. [3] Peralta G, Padrón E, Roiz MP, De Benito I, Garrido JC, Talledo F, et al. Risk factors for bacteremia in patients with limb cellulitis. Eur J Clin Microbiol Infect Dis 2006;25:619–26. [4] Carratala J, Roson B, Fernandez-Sabe N, Shaw E, Del Rio O, Rivera A, et al. Factors associated with complications and mortality in adult patients hospitalized for infectious cellulitis. Eur J Clin Microbiol Infect Dis 2003;22:151–7. [5] Gunderson CG, Martinello RA. A systematic review of bacteremias in cellulitis and erysipelas. J Infect 2012;64:148–55. [6] Dupuy A, Benchikhi H, Roujeau JC, Bernard P, Vaillant L, Chosidow O, et al. Risk factors for erysipelas of the leg (cellulitis): case–control study. BMJ 1999;318(7198):1591–4. [7] Perl B, Gottehrer NP, Raveh D, Schlesinger Y, Rudensky B, Yinnon AM. Cost-effectiveness of blood cultures for adult patients with cellulitis. Clin Infect Dis 1999;29:1483–8.
© 2017 The Authors. Published by Elsevier Ltd, NMNI, 19, 134–136 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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[8] Llop P. Genetic islands in pome fruit pathogenic and non-pathogenic Erwinia species and related plasmids. Front Microbiol 2015:6. [9] O’Hara CM, Steigerwalt AG, Hill BC, Miller JM, Brenner DJ. First report of a human isolate of Erwinia persicinus. J Clin Microbiol 1998;36: 248–50. [10] Shin SY, Lee MY, Song JH, Ko KS. New Erwinia-like organism causing cervical lymphadenitis. J Clin Microbiol 2008;46:3156–8. [11] Bläckberg A, Trell K, Rasmussen M. Erysipelas, a large retrospective study of aetiology and clinical presentation. BMC Infect Dis 2015;15:1. [12] Hauben L, Moore ER, Vauterin L, Steenackers M, Mergaert J, Verdonck L, et al. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 1998;21:384–97. [13] Stevens DL, Bisno AL, Chambers HF, Everett ED, Dellinger P, Goldstein EJ, et al. Practice guidelines for the diagnosis and
[14]
[15]
[16]
[17]
NMNI
management of skin and soft-tissue infections. Clin Infect Dis 2005;41: 1373–406. Mergaert J, Hauben L, Cnockaert MC, Swings J. Reclassification of nonpigmented Erwinia herbicola strains from trees as Erwinia billingiae sp. nov. Int J Syst Bacteriol 1999;49:377–83. Palacio-Bielsa A, Roselló M, Llop P, López MM. Erwinia spp. from pome fruit trees: similarities and differences among pathogenic and nonpathogenic species. Trees 2012;26:13–29. Kube M, Migdoll AM, Gehring I, Heitmann K, Mayer Y, Kuhl H, et al. Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genomics 2010;11:393. Umenai T, Saitoh Y, Takano S, Shoji E, Tanaka K, Ishida N. Significance of Erwinia in the vagina as causative agents of urinary tract infections. Tohoku J Exp Med 1979;129:103–4.
© 2017 The Authors. Published by Elsevier Ltd, NMNI, 19, 134–136 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
